Ascent of the Dog

Once upon a time, a few wolves gave up their freedom in exchange for our garbage. They also got smaller brains, genetic diseases, and an embarrassing array of frivolous features. In evolutionary terms, it was a terrific deal.

In the sprawling Siberian city of Novosibirsk, there's a research compound that's home to some of the world's newest and oddest dogs. They don't look odd, mind you, with their piebald coats, floppy ears, and wagging, upturned tails. They don't behave oddly, either. They wander up to the geneticists working there, yapping, sniffing, and licking their hands much as any domestic dog might do.

The reason they're remarkable is that they're not domestic dogs at all--they're silver foxes (known as red foxes in the United States), separated from Rin-Tin-Tin and Lassie by 12 million years of evolution. Prized for their fur, these wild and normally skittish animals reached their tame, doggielike state at the hands of Dmitry Belyaev, erstwhile director of the city's Institute of Cytology and Genetics. In a bid to create more manageable foxes for the fur industry, Belyaev began selectively breeding for tamer animals in 1958, transforming hostile, pointy-eared silver foxes into friendly, floppy-eared fox-dogs in a mere 20 generations.

That's how Belyaev got his version of a domesticated dog. But how did we first come by ours? We need only compare the number of chromosomes-- DNA bundles--in members of the canine family to see that our dogs aren't descended from foxes: silver foxes have just 36 chromosomes, whereas dogs have 78. Our dogs are derived from gray wolves, which not only also have 78 chromosomes but, more to the point, can still breed with dogs, making them members of the same species. Some 12,000 years ago, judging from archeological remains, these gray wolves loped into the lives of our hunter-gatherer forebears and then, over the millennia, gave rise to all the fantastic dog shapes and sizes that populate the planet today. In the United States alone an estimated 50 million dogs, from Akitas to weimaraners, now live in our homes, racking up an annual $6 billion in food bills and $4.5 billion in vet bills, and dumping a daily 20 million pounds of feces at our feet. Yet in many ways we're oddly hazy about the history of our closest animal companions. How did Canis lupus, the wolf, originate? How did he become Canis lupus familiaris, the domestic dog? And how did pugs and poodles, Lhasa apsos and Labradors come to be?

Recently the odds for cracking these mysteries have improved. Inspired by the Human Genome Project, a plan to map all the genes responsible for making a human, researchers have embarked on a similar project for the dog. One day they hope to pinpoint the genes that explain how our different breeds came about. Better still, from a canine point of view, some of this science might benefit the dogs themselves by weeding out an array of crippling genetic diseases we humans have encouraged by breeding weirder and wilder dog shapes.

Ironically, some of the earlier stages of dog evolution--before humans began manipulating the species--are becoming clearer than the later ones. All members of the dog family, including wolves, foxes, and domestic dogs, belong to the order Carnivora, a group whose hallmark is a super- specialized pair of teeth called the carnassials. Pull up your dog's lip, and you'll see them: the first molar on the lower jaw, and the last premolar on the upper jaw. They slide past each other like scissors, neatly shearing meat into chunks.

The first glimmerings of carnassials appeared in the mouths of rat-size mammals 67 million years ago, back when the dinosaurs still roamed. These ratty little animals eventually gave rise to larger carnivores, including the so-called stem dog, Hesperocyon gregarius, a slender, long-tailed animal that lived in North America's tropical forests 37 million years ago, most likely eating young birds and eggs as well as seeds and fruits. About 30 million years ago the stem-dog lineage split in two, with the dominant branch, the borophagines, growing larger and opting for an increasingly meaty diet of horses, camels, and pronghorn antelope. In most textbooks you'll still see these borophagines feted as the forerunners of our canines. In fact, recent fossil studies show that borophagines came to a sticky end, doomed by their bad food choice.

What happened, according to paleontologist Richard Tedford of the American Museum of Natural History, was that 5 million years ago, as the climate cooled, the borophagines' meat stocks dwindled. "There was no way for the borophagines to go back," says Tedford. Instead they pushed their meat-eating life-style to the limits, evolving into hulking, mastiff-size brutes with enormous, bone-crushing teeth. Much as modern hyenas follow lions, borophagines tagged behind saber-toothed cats, crunching the carcasses left by the cats to slurp fatty marrow from the bones. Even so, 2.5 million years ago, the last borophagines gave up the ghost.

Their loss was Lassie's gain. Waiting in the wings was that other stem-dog offshoot, Leptocyon, and it's this line that led to our modern canines. Unlike the latter-day borophagines, Leptocyon was a slender, narrow-snouted carnivore. Its teeth had no special bone-crushing adaptations. Leptocyon made use of two small cusps at the back of its lower carnassials for crushing plant matter, allowing it (like Hesperocyon) to eat berries and fruits as well as rodents and rabbits. All members of the modern dog family have retained this useful diet-diversifying feature. "It's a great adaptation," says Tedford. "Think of foxes--they have a very mixed diet, and that's one reason they're great survivors. They can raid your garbage can, and they'll eat berries and fruits and plants and insects and whatever they can get." That unpicky diet was to be a key to canine evolutionary success.

"As borophagines waned, the diversity of canines was released," says Tedford. "Whereas there was just Leptocyon before--suddenly, whammo!" In a few million years wolves and foxes had evolved and were diversifying like crazy. They poured into the Old World via the Bering land bridge; they changed their minds and trotted back to America again; they trickled down to South America. Then, 12,000 years ago, the gray wolf entered our domestic lives.

There are any number of accounts of how the wolf came to stay. Perhaps Stone Age villagers brought wolf pups back to the camp and kept them as pets or guard dogs; perhaps they used them as a handy food source, or trained them for the hunt. "It's sort of a never-ending controversy," says James Serpell, an animal behaviorist at the University of Pennsylvania. "People can't help speculating about how the dog got domesticated, but they're all 'Just So' stories."

Raymond Coppinger's story is that people initially had little to do with it--dogs domesticated themselves to get at our trash. "There's pretty good evidence for this," says Coppinger, an animal behaviorist at Hampshire College in Amherst, Massachusetts. "If you look at wildlife in Alaska today, if you look at wolves in Italy, you'll always see wolves at a dump because dumps are good places for food." Belyaev's fox experiment, Coppinger believes, supports his contention, since essentially what Belyaev did was select for "short flight distance"--for animals that let people get close before they ran away. In the "village dump" scenario, the ability to root through garbage without skittering away every time a human came along would have been just the ticket. Fearless wolves got the most food and left the most offspring. Just as Belyaev's foxes got tamer and tamer through the generations, so did the wolves. Eventually they didn't even pass for bona fide wolves anymore. They were something new--the world's first domestic dogs.

Of course, Belyaev got more than tameness in his foxes. He also got those other things: multicolored fur, yapping, and tail wagging. The colorful fur, incidentally, ruled out the idea of using fox-dogs as nice, manageable animals on fur farms--from a fashion point of view, piebald coats just didn't cut it. But the experiment was satisfying from a scientific point of view, since dogs, too, have those traits. Why on earth did they happen?

The explanation Belyaev, Coppinger, and others have come up with goes something like this: Foxes and wolves, like us, go through hugely different stages as they grow--stages crisply orchestrated by genes turning on and off at crucial moments in development. Your average fox pup is a trusting, attention-seeking little animal, programmed to solicit care from its mother. Your average adult fox is a wary critter, as befits a wild animal in a world full of dangers. So maybe the easiest way to get tameness is to breed a Peter Pan-like fox--one whose genetic timing has been delayed and whose puppylike trust persists into adulthood.

At the start of the experiment, the foxes you pick to mate with each other may have just slightly delayed development. But by selecting and mating the tamest animals in every generation, you'll eventually end up with something really Peter Pan-like--a fox-dog. And since you've messed with the animals' developmental clock, you'll most likely end up with other puppy traits too--yapping, whining, tail wagging. You'll even end up with brand-new traits, like colored coats. Melanin, a skin and fur pigment, is produced from the same chemical--dopa--that's used to make the neurochemical dopamine, as well as other key chemicals. When you select for altered behavior, you could also be getting altered dopamine production. "And once you fool around with the dopa pathway, there's a good chance you'll mess up the melanin pathway too," says Coppinger.

No wonder domestic dogs act so geeky--whining, chasing sticks, ripping slippers to shreds. In some ways they're no more than adolescent wolves. (A 100-pound wolf has a 400-cubic-centimeter brain, says Coppinger, while a comparable dog has a 250 cc brain, which supports the notion that we've selected for dogs stuck with wolf-puppy brains.) Belyaev's experiment in selection, then, appears to explain the development of those first friendly wolf-dogs. Might it also shed light on how humans arrived at the vast array of breeds we see today?

Think of them all--all those retrievers and sheepdogs, terriers and hounds, 136 breeds recognized by the American Kennel Club and many more waiting for its seal of approval. Today we enjoy them for their companionship and for their pleasing shapes and forms, but--this much we can glean from historical artifacts and records--the first breeds were usually crafted for work. Without knowing a thing about genetics, early dog fanciers apparently looked at whatever wolf-descended mutts were available to them, picking out those with a talent for herding or retrieving or sniffing or running. They then bred their selections, getting better and better performers down through the generations. Eventually they produced the border collie, whose obsessive urge to herd is so handy with sheep; the dachshund, whose elongated body and stubby legs suited it for hunting badgers in their holes; the bloodhound, whose heightened sense of smell tracks down foxes and fugitives.

Bob Wayne, an evolutionary biologist at UCLA, has an inkling of the genetic differences those early breeders tapped into. Again, developmental timing à la Belyaev seems to be involved. In the late 1980s Wayne published a slew of bone measurements suggesting that altered developmental timing--which gave us our dogs in the first place--is also key to all the canine variety we see today. All pups, no matter what the breed, start out looking pretty much the same. Slow down their growth, or stop that growth a little earlier, and you'll end up with a dog more puplike in shape, like a West Highland white terrier. Speed up that clock, or let them continue growing, and you'll end up with some sort of "hyperdog" like a Great Dane. Settle for a sensible, in-between growth rate, and you'll get the sensible, in-between proportions of a retriever.

Wayne argues that you couldn't get all this variety from breed to breed if the puppy wasn't so profoundly different in shape from the grown dog--compare the pup's squat skull with the adult's slender snouted one, for example. That great difference means you can get any number of dog shapes by halting growth at different points along the developmental pathway. Kittens and cats, on the other hand, are pretty similar in shape-- and that's reflected in cat breeds, which are much of a muchness, except for their striking fur variations. "If you just ask cats not to grow as much, or as fast, you'll still come up with a cat that looks like a cat," Wayne says.

Could similar clock manipulations--as Belyaev's experiment also seems to hint--lie behind a breed's behavior? Coppinger, for one, thinks they might. For example, sheep herders, such as border collies, display many "grown-up" hunting behaviors--they stalk, chase, and bite the sheep (but handily stop short of killing). Sheep-guarding dogs like the Italian maremma are a different matter. They move with the flock and play with the sheep like puppies. But precisely which genes are orchestrating these adult and puppyish behaviors is anybody's guess. The genes responsible for most dog traits remain utterly mysterious.

So do the origins of most lineages. A wall chart sketching a family tree of dog breeds is slapped up in many a dog researcher's lab, but it's largely hokum. Turn to the dog books, and time and again you'll read of breeds, depicted in ancient frescoes, whose origins "are lost in the mists of time." Furthermore, it's not as if all ancient breeds have remained pure since those distant days; many a nineteenth-century breeder added a dash of spaniel or a pinch of poodle to the equation.

These days, you'd imagine that molecular biology could ride in on its white charger and sort out the mess in a twinkling. Think again, says evolutionary geneticist Rodney Honeycutt, of Texas A&M.; Five years ago his lab began to try to figure out the relationships between 28 canine breeds by comparing their DNA. Distantly related breeds, the researchers reasoned, would have the most dissimilar DNA, and closely related breeds, the most similar. And so they selected bits of DNA from each dog and compared the sequences of their building blocks--the nucleotides A, C, T, and G. "It was a mess," reports Honeycutt. "We couldn't even group individuals of a breed together." Only one breed, the maremma, stood out from the rest. You couldn't even tell a dog breed like a springer spaniel from a wolf.

In the long run, though, molecular biology could clear the waters. Jasper Rine, a geneticist at the University of California at Berkeley, has made it his mission to find the genes responsible for the "evolution" of dog breeds. Three years ago Rine, working with Elaine Ostrander, now at the University of Washington, and George Sprague at the University of Oregon, launched his dog genome project.

Studying dogs, says Rine, is a fabulous way to get at the genes behind the differences in behavior and body shape that Darwin so eloquently described in Origin of Species as driving evolution. After all, the prime way to understand genes is to cross different "types" and assess the offspring, just as the monk Gregor Mendel did with different peas. You can't make genetic crosses between species--by and large, they can't interbreed. With the dog, though, you've got all that variety in shape and temper and you can breed anything with anything. "With dogs we can bring together the two great ideas in biology--those of Darwin and those of Mendel," Rine says. "It's a laboratory of evolution at our disposal."

The dogs currently under study are a border collie named Gregor and a Newfoundland named Pepper, owned by Rine and his wife. On a typical day, Gregor and Pepper pass their time in Rine's office in the university's aptly named Barker Hall. Gregor--named after Mendel, naturally--hunkers at Rine's feet as he taps away on his computer keyboard. Pepper sprawls on the floor like a large, lumpy rug. Both are key to the Big Experiment, which will pinpoint the genes responsible for the dogs' distinctly different shapes, sizes, and behaviors.

Gregor, for instance, is a svelte dog, weighing 37 pounds to Pepper's hefty 99. His coat is black with white at the neck, nose, paws, and tail tip; Pepper's is pure black. As befits a collie, Gregor has a hypnotic stare and an instinct to herd--he plays fetch with a passion. As befits a Newfoundland, Pepper has webbed feet, loves water, and displays her breed's water-rescue skills--many a Newfie has saved a drowning human. She couldn't care less about fetch, though.

To tease all these traits apart at the genetic level, Rine's first step was to mate Pepper with Gregor. A total of seven Pepper-Gregor offspring are already residing as pets in Bay Area and Seattle homes. Their weight is midway between that of their parents, and they have black coats with bits of white. They love water--and their feet are most definitely webbed. They like fetch, but they don't stare down tennis balls the way their father does.

These dogs are pretty similar, as you'd expect when crossing one pure line with another. But now brothers and sisters are being mated, and their offspring--nine were born this summer--should include dogs widely varying in shape, size, and temperament. Here the experiment truly begins, because it's only when you have dogs that differ from one another that you can start to link particular traits to particular genes.

To do their analysis, Rine and company estimate they'll need a motley collection of up to 150 animals. They'll look at the animals' size, coat color, water-rescue skills, and so on and then try to match those traits to differences in the dogs' DNA. That's no easy task, since the dog genome is large and uncharted. So while breeding proceeds, the team is working fiercely to piece together a first map of that genome, using DNA extracted from Gregor's and Pepper's blood cells.

What's needed, says Ostrander, Rine's colleague in mapping, are little molecular signposts spaced up and down the dog's chromosomes, like signposts along U.S. highways. "Imagine trying to get from San Francisco to Poughkeepsie, New York, without knowing anything about the space in between," she says. "If you were just wandering randomly, in about a billion years you might land in Poughkeepsie. But if someone gave you a map that had a landmark every hundred miles, then you'd know the next logical direction to proceed. When you're looking for genes, a genetic map does exactly the same thing."

The signposts--known as microsatellites--are small stretches of DNA in which a simple string of DNA building blocks--such as CACACACACA--is repeated over and over again. The handy thing about the repeats is that, first of all, they crop up all over the genome, and second, the number of CAs in a given repeat will vary between individual dogs. Let's suppose Gregor has a pal, Slasher the pit bull, with a 17-CA repeat at the tip of her chromosome 16. Another buddy, Felix the toy poodle, has 15 CAs at the same site. You can tell the two apart because the small piece of DNA containing Slasher's repeat is slightly larger than the DNA containing Felix's, by virtue of those two extra CAs. You'd see differences like this with lots of repeats at lots of sites all over Slasher's and Felix's genomes.

Now let's suppose that Felix is an incessant yapper and that no quantity of minced-chicken bonbons will cure him of the habit. Slasher, meanwhile, is the solid, silent type. You mate Felix and Slasher and then duly note the temperament of their descendants. At the same time, you study the descendants' DNA, and here's what you see: even though the DNA from Slasher and Felix gets mixed and jumbled through the generations, and their CA repeats along with it, there is one clear-as-a-bell pattern that emerges. Every yapping dog has a Felix-style repeat at the tip of chromosome 16, and every silent dog has Slasher's repeat there. Aha! you conclude. There's most likely a gene that influences yapping on chromosome 16, sitting close to that repeat, and (to cut a long and complicated story short) you can find it and clone it.

Of course, Rine, Sprague, and Ostrander would happily chew up a squeak-bone apiece if it turns out to be that simple for Pepper's water skills or Gregor's herding. They know that complex behaviors are probably influenced by many genes, and that differences in the puppies' environments will muddy matters even more.

Mapping the dog genome should in the end pay off not only for the researchers but also for the dogs, by helping redress the wrongs our breeding experiments have wrought. If dogs have a bone to pick with people, if they have cause to regret their domestication, they need only point to the genetic diseases plaguing different breeds today--clotting disorders, hip deformities, progressive blindness, and more. Felix the poodle could give you an earful about his dislocated kneecaps. Slasher the pit bull could respectfully request an accounting of her chronic deafness. In some cases the numbers of affected dogs are staggering. One in four Bedlington terriers will get copper toxicosis, a liver-damaging ailment that's fatal when untreated. And all these ailments stem from the very same strategy that makes purebred breeds "pure"--inbreeding. We frown on it in humans for a reason.

Let's say you're a dog breeder and you've stumbled on a nifty new twisty tail in a collie. "Right," you say. "I'll set up a new line." But you don't have many twisty-tailed dogs, so you cross those few together and soon your place is crawling with twisty-tails. And maybe one dog has a gloriously twisty tail, so you use him as stud dog again and again to enhance your stock. The tails gets twistier, the stock gets purer--but what you didn't know was that the dog carried some nasty baggage, a recessive gene causing blindness. He wasn't blind: he had only one copy of the bad gene, and it takes two to get the disease. But now you've poured that bad gene into your stock, and lots of the dogs get two copies. Blind dogs start cropping up all over.

Granted, breeders would be hard-pressed to keep their lines pure or start new ones if they couldn't do some inbreeding. What's the answer? In part, it's old-fashioned genetic counseling--figuring out the genetics from family trees, pinpointing likely carriers of a bad gene, and advising dog owners not to breed those animals. Today there's a real effort to do this. For the last five years, in Davis, California, the Institute for Genetic Disease Control in Animals has run an open registry for genetic diseases, in which anyone (not just the owner) can look up a dog to see whether it's diseased or a disease-gene carrier.

In the future, though, the answer will probably lie in DNA diagnostics. Researchers led by George Brewer, a medical geneticist at the University of Michigan, are pursuing a dog genome project for just this purpose, spinning off their efforts into a private company, Vetgen. In Brewer's scheme, breeders will provide family trees for a particular lineage of diseased dogs. His team will extract DNA from dogs in that family and (using the same strategy adopted by Rine) search for a microsatellite repeat tightly linked to the disease gene. Once one is found, breeders should be able to send in DNA samples for any new dogs in the family and learn what their dog's disease status is. Breeders will then be able to weed out the bad gene by not mating affected animals.

Weed out the bad genes, and life for dogs would certainly look up. But it would still be a dog's life. True, there's shelter; frequent and well-balanced meals; love, care, and attention. Still, nearly one-third of U.S. dogs end their days in animal shelters--and let's not forget neutering, animal experimentation, arbitrary standards for tail-cutting in many breeds, and that dog in many parts of the world means lunch.

And then, what of freedom? Dignity? You have to wonder if Felix or Slasher ever stares wistfully out the window, faced with all those stern little lectures about getting into the garbage, all that trotting to heel and shaking paws, to say nothing of the indignities of fluffed-up pom-poms and little tartan overcoats. Then, ah, the life of the wolf--coursing through the forest with your pack mates, the wind in your fur, howling at the moon high above the sparkling, snow-clad tundra. . . . If dogs really did domesticate themselves, did they make a prudent choice?

James Serpell of the University of Pennsylvania isn't sure. "There's this extraordinary ambivalence about dogs worldwide--they go from being treated as pariahs to being treated as closest relatives and best friends," he says. "If you're lucky and get a decent owner who likes dogs for their dogginess and appreciates the kinds of things dogs like doing, then you're going to have a really good life. But too many dogs find themselves owned by people who are ignorant or irresponsible, people who are using them as fashion accessories or to express some bizarre aspect of their own personality. And remember--dogs in most parts of the world have a rough deal. They scavenge to survive. They're diseased. They're short- lived."

But then the life of a wolf is no bed of roses either. And it's getting tougher all the time, as humans move into every last wild place on Earth, carving up once-massive ranges into isolated pockets that no longer support a proper wolf pack. Given the runaway success of our species, maybe dogs were wise to hitch their fate to ours, after all. Right now a hard- boiled evolutionary judgment would have to crown Rover, not White Fang, lord of the dogs. "There may be 38,000 wolves left in North America," says Coppinger, "while in the U.S. there are something like 50 million domestic dogs. Whose DNA has been more successful? Does DNA care about freedom? If you just boil it down to pounds of dog and pounds of wolf, then the dog wins every time."